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      Associations between Parity, Hair Hormone Profiles during Pregnancy and Lactation, and Infant Development in Rhesus Monkeys ( Macaca mulatta)

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          Abstract

          Studies examining hormones throughout pregnancy and lactation in women have been limited to single, or a few repeated, short-term measures of endocrine activity. Furthermore, potential differences in chronic hormonal changes across pregnancy/lactation between first-time and experienced mothers are not well understood, especially as they relate to infant development. Hormone concentrations in hair provide long-term assessments of hormone production, and studying these measures in non-human primates allows for repeated sampling under controlled conditions that are difficult to achieve in humans. We studied hormonal profiles in the hair of 26 female rhesus monkeys ( Macaca mulatta, n=12 primiparous), to determine the influences of parity on chronic levels of cortisol (hair cortisol concentration, HCC) and progesterone (hair progesterone concentration, HPC) during early- to mid-pregnancy (PREG1), in late pregnancy/early lactation (PREG2/LACT1), and in peak lactation (LACT2). We also assessed infants’ neurobehavioral development across the first month of life. After controlling for age and stage of pregnancy at the first hair sampling period, we found that HCCs overall peaked in PREG2/LACT1 (p=0.02), but only in primiparous monkeys (p<0.001). HPCs declined across pregnancy and lactation for all monkeys (p<0.01), and primiparous monkeys had higher HPCs overall than multiparous monkeys (p=0.02). Infants of primiparous mothers had lower sensorimotor reflex scores (p=0.02) and tended to be more irritable (p=0.05) and less consolable (p=0.08) in the first month of life. Moreover, across all subjects, HCCs in PREG2/LACT1 were positively correlated with irritability (r (s)=0.43, p=0.03) and negatively correlated with sensorimotor scores (r (s)=-0.41, p=0.04). Together, the present results indicate that primiparity influences both chronic maternal hormonal profiles and infant development. These effects may, in part, reflect differential reproductive and maternal effort in mothers with varied caretaking experience. In addition, infant exposure to relatively higher levels of maternal cortisol during the late fetal and early postnatal periods is predictive of poorer developmental outcomes.

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          The timing of prenatal exposure to maternal cortisol and psychosocial stress is associated with human infant cognitive development.

          The consequences of prenatal maternal stress for development were examined in 125 full-term infants at 3, 6, and 12 months of age. Maternal cortisol and psychological state were evaluated 5 times during pregnancy. Exposure to elevated concentrations of cortisol early in gestation was associated with a slower rate of development over the 1st year and lower mental development scores at 12 months. Elevated levels of maternal cortisol late in gestation, however, were associated with accelerated cognitive development and higher scores at 12 months. Elevated levels of maternal pregnancy-specific anxiety early in pregnancy were independently associated with lower 12-month mental development scores. These data suggest that maternal cortisol and pregnancy-specific anxiety have programming influences on the developing fetus.
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            Psychosocial stress and pregnancy outcome.

            This article is intended to help clinicians better understand the ever-expanding body of research on whether psychosocial stress (both acute and chronic) is linked to 2 major adverse pregnancy outcomes: preterm birth and low birth weight. We summarize the existing literature and then review assessment tools commonly used to diagnose various types of psychosocial stress, with attention to how and when assessments should be made. After discussing the physiologic mechanisms hypothesized to underlie these relationships, we examine the range of existing interventions aimed at reducing psychosocial stress and review their efficacy at improving birth outcomes. Future directions for prevention of adverse pregnancy outcomes are discussed and suggest that an entirely new approach may be necessary.
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              Prenatal exposure to maternal depression and cortisol influences infant temperament.

              Accumulating evidence indicates that prenatal maternal and fetal processes can have a lasting influence on infant and child development. Results from animal models indicate that prenatal exposure to maternal stress and stress hormones has lasting consequences for development of the offspring. Few prospective studies of human pregnancy have examined the consequences of prenatal exposure to stress and stress hormones. In this study the effects of prenatal maternal psychosocial (anxiety, depression, and perceived stress) and endocrine (cortisol) indicators of stress on infant temperament were examined in a sample of 247 full-term infants. Maternal salivary cortisol and psychological state were evaluated at 18-20, 24-26, and 30-32 weeks of gestation and at 2 months postpartum. Infant temperament was assessed with a measure of negative reactivity (the fear subscale of the Infant Temperament Questionnaire) at 2 months of age. Elevated maternal cortisol at 30-32 weeks of gestation, but not earlier in pregnancy, was significantly associated with greater maternal report of infant negative reactivity. Prenatal maternal anxiety and depression additionally predicted infant temperament. The associations between maternal cortisol and maternal depression remained after controlling for postnatal maternal psychological state. These data suggest that prenatal exposure to maternal stress has consequences for the development of infant temperament.
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                Author and article information

                Contributors
                Role: Editor
                Journal
                PLoS One
                PLoS ONE
                plos
                plosone
                PLoS ONE
                Public Library of Science (San Francisco, CA USA )
                1932-6203
                14 July 2015
                2015
                : 10
                : 7
                : e0131692
                Affiliations
                [1 ]Laboratory of Comparative Ethology, Eunice Kennedy Shriver National Institute of Child Health & Human Development, NIH, Poolesville, Maryland, United States of America
                [2 ]Department of Psychological and Brain Sciences, University of Massachusetts Amherst, Amherst, Massachusetts, United States of America
                INRA, FRANCE
                Author notes

                Competing Interests: The authors have declared that no competing interests exist.

                Conceived and designed the experiments: AMD MAN JSM. Performed the experiments: AMD KLR. Analyzed the data: AMD. Contributed reagents/materials/analysis tools: MAN JSM SJS. Wrote the paper: AMD KLR JSM.

                Article
                PONE-D-15-14865
                10.1371/journal.pone.0131692
                4501543
                26172048
                202b4963-1630-48c8-95b0-baa56ff1ef7e

                This is an open access article, free of all copyright, and may be freely reproduced, distributed, transmitted, modified, built upon, or otherwise used by anyone for any lawful purpose. The work is made available under the Creative Commons CC0 public domain dedication

                History
                : 6 April 2015
                : 5 June 2015
                Page count
                Figures: 5, Tables: 1, Pages: 16
                Funding
                SJS: Eunice Kennedy Shriver National Institute of Child Health & Human Development Division of Intramural Research Grant #HD001106 https://dir.nichd.nih.gov/dirweb/home.html. MAN: National Institutes of Health Grant #OD011180 http://www.nih.gov/about/almanac/organization/NCRR.htm.
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